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General Review Article

Limb-girdle Muscular Dystrophy and Therapy: Insights into Cell and Gene-based Approaches

Author(s): Forough Taheri, Eskandar Taghizadeh, Mohammad J.R. Pour, Daryoush Rostami, Pedram G. Renani, Azam Rastgar-Moghadam and Seyed M.G. Hayat*

Volume 19, Issue 6, 2019

Page: [386 - 394] Pages: 9

DOI: 10.2174/1566523220666200218113526

Price: $65

Abstract

The Limb-Girdle Muscular Dystrophies (LGMD) are genetically heterogeneous disorders, responsible for muscle wasting and severe form of dystrophies. Despite the critical developments in the insight and information of pathomechanisms of limb-girdle muscular dystrophy, any definitive treatments do not exist, and current strategies are only based on the improvement of the signs of disorder and to enhance the life quality without resolving an underlying cause. There is a crucial relationship between pharmacological therapy and different consequences; therefore, other treatment strategies will be required. New approaches, such as gene replacement, gene transfer, exon skipping, siRNA knockdown, and anti-myostatin therapy, which can target specific cellular or molecular mechanism of LGMD, could be a promising avenue for the treatment. Recently, genome engineering strategies with a focus on molecular tools such as CRISPR-Cas9 are used to different types of neuromuscular disorders and show the highest potential for clinical translation of these therapies. Thus, recent advancements and challenges in the field will be reviewed in this paper.

Keywords: Adeno-associated virus, exon skipping, gene therapy, limb-girdle muscular dystrophy, LGMD, gene editing.

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[1]
Walton JN, Nattrass FJ. On the classification, natural history and treatment of the myopathies. Brain 1954; 77(2): 169-231.
[http://dx.doi.org/10.1093/brain/77.2.169] [PMID: 13190076]
[2]
Straub V, Murphy A, Udd B. 229th ENMC international workshop: Limb girdle muscular dystrophies - Nomenclature and reformed classification Naarden, the Netherlands, 17-19 March 2017. Neuromuscul Disord 2018; 28(8): 702-10.
[http://dx.doi.org/10.1016/j.nmd.2018.05.007] [PMID: 30055862]
[3]
Thompson R, Straub V. Limb-girdle muscular dystrophies - international collaborations for translational research. Nat Rev Neurol 2016; 12(5): 294-309.
[http://dx.doi.org/10.1038/nrneurol.2016.35] [PMID: 27033376]
[4]
Norwood FL, Harling C, Chinnery PF, Eagle M, Bushby K, Straub V. Prevalence of genetic muscle disease in Northern England: In depth analysis of a muscle clinic population. Brain 2009; 132(Pt 11): 3175-86.
[http://dx.doi.org/10.1093/brain/awp236] [PMID: 19767415]
[5]
Mahmood OA, Jiang XM. Limb-girdle muscular dystrophies: where next after six decades from the first proposal (Review). Mol Med Rep 2014; 9(5): 1515-32.
[http://dx.doi.org/10.3892/mmr.2014.2048] [PMID: 24626787]
[6]
Magri F, Del Bo R, D’Angelo MG, et al. Frequency and characterisation of anoctamin 5 mutations in a cohort of Italian limb-girdle muscular dystrophy patients. Neuromuscul Disord 2012; 22(11): 934-43.
[http://dx.doi.org/10.1016/j.nmd.2012.05.001] [PMID: 22742934]
[7]
Lo HP, Cooper ST, Evesson FJ, et al. Limb-girdle muscular dystrophy: diagnostic evaluation, frequency and clues to pathogenesis. Neuromuscul Disord 2008; 18(1): 34-44.
[http://dx.doi.org/10.1016/j.nmd.2007.08.009] [PMID: 17897828]
[8]
Bönnemann CG, Wang CH, Quijano-Roy S, et al. Diagnostic approach to the congenital muscular dystrophies. Neuromuscul Disord 2014; 24(4): 289-311.
[http://dx.doi.org/10.1016/j.nmd.2013.12.011] [PMID: 24581957]
[9]
Herrmann R, Straub V, Blank M, et al. Dissociation of the dystroglycan complex in caveolin-3-deficient limb girdle muscular dystrophy. Hum Mol Genet 2000; 9(15): 2335-40.
[http://dx.doi.org/10.1093/oxfordjournals.hmg.a018926] [PMID: 11001938]
[10]
Moreira ES, Wiltshire TJ, Faulkner G, et al. Limb-girdle muscular dystrophy type 2G is caused by mutations in the gene encoding the sarcomeric protein telethonin. Nat Genet 2000; 24(2): 163-6.
[http://dx.doi.org/10.1038/72822] [PMID: 10655062]
[11]
Servián-Morilla E, Takeuchi H, Lee TV, et al. A POGLUT1 mutation causes a muscular dystrophy with reduced Notch signaling and satellite cell loss. EMBO Mol Med 2016; 8(11): 1289-309.
[http://dx.doi.org/10.15252/emmm.201505815] [PMID: 27807076]
[12]
Scrivens PJ, Shahrzad N, Moores A, Morin A, Brunet S, Sacher M. TRAPPC2L is a novel, highly conserved TRAPP-interacting protein. Traffic 2009; 10(6): 724-36.
[http://dx.doi.org/10.1111/j.1600-0854.2009.00906.x] [PMID: 19416478]
[13]
Schindler RF, Scotton C, Zhang J, et al. POPDC1(S201F) causes muscular dystrophy and arrhythmia by affecting protein trafficking. J Clin Invest 2016; 126(1): 239-53.
[http://dx.doi.org/10.1172/JCI79562] [PMID: 26642364]
[14]
Izumi R, Niihori T, Takahashi T, et al. Genetic profile for suspected dysferlinopathy identified by targeted next-generation sequencing. Neurol Genet 2015; 1(4): e36
[http://dx.doi.org/10.1212/NXG.0000000000000036] [PMID: 27066573]
[15]
Taghizadeh E, Rezaee M, Barreto GE, Sahebkar A. Prevalence, pathological mechanisms, and genetic basis of limb-girdle muscular dystrophies: A review. J Cell Physiol 2019; 234(6): 7874-84.
[http://dx.doi.org/10.1002/jcp.27907] [PMID: 30536378]
[16]
Straub V, Murphy A, Udd B. LGMD workshop study group; 229th ENMC international workshop: Limb girdle muscular dystrophies - Nomenclature and reformed classification Naarden, the Netherlands, 17-19 March 2017. The Netherlands. . Neuromuscul Disord 2018; 28(8): 702-10.
[http://dx.doi.org/10.1016/j.nmd.2018.05.007]
[17]
Taghizadeh E, Abdolkarimi H, Boostani R, Sadrnabavi A. Limb-girdle muscular dystrophy with new mutation in sarcoglycan beta gene: A case report. Iran J Public Health 2018; 47(12): 1953-7.
[PMID: 30788312]
[18]
Straub V, Bushby K. Therapeutic possibilities in the autosomal recessive limb-girdle muscular dystrophies. Neurotherapeutics 2008; 5(4): 619-26.
[http://dx.doi.org/10.1016/j.nurt.2008.08.003] [PMID: 19019315]
[19]
Wicklund MP, Kissel JT. The limb-girdle muscular dystrophies. Neurol Clin 2014; 32(3): 729-49. , ix
[http://dx.doi.org/10.1016/j.ncl.2014.04.005] [PMID: 25037088]
[20]
Topaloglu H. Evidence-based guideline summary: Diagnosis and treatment of limb-girdle and distal dystrophies: Report of the guideline development subcommittee of the American Academy of Neurology and the practice issues review panel of the American Association of Neuromuscular & electrodiagnostic medicine. Neurology 2015; 84(16): 1720.
[http://dx.doi.org/10.1212/WNL.0000000000001508] [PMID: 25901060]
[21]
Angelini C, Giaretta L, Marozzo R. An update on diagnostic options and considerations in limb-girdle dystrophies. Expert Rev Neurother 2018; 18(9): 693-703.
[http://dx.doi.org/10.1080/14737175.2018.1508997] [PMID: 30084281]
[22]
Serafini PR, Feyder MJ, Hightower RM, et al. A limb-girdle muscular dystrophy 2I model of muscular dystrophy identifies corrective drug compounds for dystroglycanopathies. JCI Insight 2018; 3(18): 120493
[http://dx.doi.org/10.1172/jci.insight.120493] [PMID: 30232282]
[23]
Wong-Kisiel LC, Kuntz NL. Two siblings with limb-girdle muscular dystrophy type 2E responsive to deflazacort. Neuromuscul Disord 2010; 20(2): 122-4.
[http://dx.doi.org/10.1016/j.nmd.2009.11.005] [PMID: 20071171]
[24]
Darin N, Kroksmark AK, Ahlander AC, Moslemi AR, Oldfors A, Tulinius M. Inflammation and response to steroid treatment in limb-girdle muscular dystrophy 2I. Eur J Paediatr Neurol 2007; 11(6): 353-7.
[http://dx.doi.org/10.1016/j.ejpn.2007.02.018] [PMID: 17446099]
[25]
Quattrocelli M, Salamone IM, Page PG, Warner JL, Demonbreun AR, McNally EM. Intermittent glucocorticoid dosing improves muscle repair and function in mice with limb-girdle muscular dystrophy. Am J Pathol 2017; 187(11): 2520-35.
[http://dx.doi.org/10.1016/j.ajpath.2017.07.017] [PMID: 28823869]
[26]
Domingos J, Sarkozy A, Scoto M, Muntoni F. Dystrophinopathies and limb-girdle muscular dystrophies. Neuropediatrics 2017; 48(4): 262-72.
[http://dx.doi.org/10.1055/s-0037-1601860] [PMID: 28427100]
[27]
Wu B, Shah SN, Lu P, et al. Long-term treatment of tamoxifen and raloxifene alleviates dystrophic phenotype and enhances muscle functions of FKRP dystroglycanopathy. Am J Pathol 2018; 188(4): 1069-80.
[http://dx.doi.org/10.1016/j.ajpath.2017.12.011] [PMID: 29571322]
[28]
Mendell JR, Rodino-Klapac L, Sahenk Z, et al. Gene therapy for muscular dystrophy: lessons learned and path forward. Neurosci Lett 2012; 527(2): 90-9.
[http://dx.doi.org/10.1016/j.neulet.2012.04.078] [PMID: 22609847]
[29]
Masakazu Saitoh M, Ishida J, Ebner N, Anker SD, Springer J, von Haehling S. Myostatin inhibitors as pharmacological treatment for muscle wasting and muscular dystrophy. JCSM Clin Rep 2017; 2(1): 1-10.
[http://dx.doi.org/10.17987/jcsm-cr.v2i1.37]
[30]
Mariot V, Joubert R, Hourdé C, et al. Downregulation of myostatin pathway in neuromuscular diseases may explain challenges of anti-myostatin therapeutic approaches. Nat Commun 2017; 8(1): 1859.
[http://dx.doi.org/10.1038/s41467-017-01486-4] [PMID: 29192144]
[31]
Wagner KR, Fleckenstein JL, Amato AA, et al. A phase I/IItrial of MYO-029 in adult subjects with muscular dystrophy. Ann Neurol 2008; 63(5): 561-71.
[http://dx.doi.org/10.1002/ana.21338] [PMID: 18335515]
[32]
Garber K. No longer going to waste. Nat Biotechnol 2016; 34(5): 458-61.
[http://dx.doi.org/10.1038/nbt.3557] [PMID: 27153267]
[33]
Campbell C, McMillan HJ, Mah JK, et al. Myostatin inhibitor ACE-031 treatment of ambulatory boys with Duchenne muscular dystrophy: Results of a randomized, placebo-controlled clinical trial. Muscle Nerve 2017; 55(4): 458-64.
[http://dx.doi.org/10.1002/mus.25268] [PMID: 27462804]
[34]
Sharma A, Badhe P, Sane H, Gokulchandran N, Paranjape A. In: Role of stem cell therapy in treatment of muscular dystrophy. India: Neuro Gen Brain & Spine Institute 2016; pp. 1-22.
[35]
Sandonà D, Betto R. Sarcoglycanopathies: molecular pathogenesis and therapeutic prospects. Expert Rev Mol Med 2009; 11: e28
[http://dx.doi.org/10.1017/S1462399409001203] [PMID: 19781108]
[36]
Torrente Y, Belicchi M, Sampaolesi M, et al. Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 2004; 114(2): 182-95.
[http://dx.doi.org/10.1172/JCI20325] [PMID: 15254585]
[37]
Price FD, Kuroda K, Rudnicki MA. Stem cell based therapies to treat muscular dystrophy. Biochim Biophys Acta 2007; 1772(2): 272-83.
[http://dx.doi.org/10.1016/j.bbadis.2006.08.011] [PMID: 17034994]
[38]
Le Grand F, Rudnicki M. Satellite and stem cells in muscle growth and repair. Development 2007; 134(22): 3953-7.
[http://dx.doi.org/10.1242/dev.005934] [PMID: 17965049]
[39]
Vilquin JT. Myoblast transplantation: clinical trials and perspectives. Mini-review. Acta Myol 2005; 24(2): 119-27.
[PMID: 16550929]
[40]
Skuk D, Goulet M, Roy B, et al. First test of a “high-density injection” protocol for myogenic cell transplantation throughout large volumes of muscles in a Duchenne muscular dystrophy patient: eighteen months follow-up. Neuromuscul Disord 2007; 17(1): 38-46.
[http://dx.doi.org/10.1016/j.nmd.2006.10.003] [PMID: 17142039]
[41]
Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998; 279(5356): 1528-30.
[http://dx.doi.org/10.1126/science.279.5356.1528] [PMID: 9488650]
[42]
Sharma A, Sane H, Gokulchandran N, et al. The role of cell transplantation in modifying the course of limb girdle muscular dystrophy: A longitudinal 5-year study. Degener Neurol Neuromuscul Dis 2015; 5: 93-102.
[http://dx.doi.org/10.2147/DNND.S71775]
[43]
Ullah I, Subbarao RB, Rho GJ. Human mesenchymal stem cells - current trends and future prospective. Biosci Rep 2015; 35(2)e00191
[http://dx.doi.org/10.1042/BSR20150025] [PMID: 25797907]
[44]
Xiong F, Xu Y, Zheng H, et al. Microdystrophin delivery in dystrophin-deficient (mdx) mice by genetically-corrected syngeneic MSCs transplantation. Transplant Proc 2010; 42(7): 2731-9.
[http://dx.doi.org/10.1016/j.transproceed.2010.04.031] [PMID: 20832578]
[45]
Xin Y, Wang YM, Zhang H, et al. Aging adversely impacts biological properties of human bone marrow-derived mesenchymal stem cells: implications for tissue engineering heart valve construction. Artif Organs 2010; 34(3): 215-22.
[http://dx.doi.org/10.1111/j.1525-1594.2009.00824.x] [PMID: 19392880]
[46]
Vieira NM, Bueno CR Jr, Brandalise V, et al. SJL dystrophic mice express a significant amount of human muscle proteins following systemic delivery of human adipose-derived stromal cells without immunosuppression. Stem Cells 2008; 26(9): 2391-8.
[http://dx.doi.org/10.1634/stemcells.2008-0043] [PMID: 18583542]
[47]
Yu J, Thomson JA. Induced pluripotent stem cells Principles of Tissue Engineering. 4th ed. Boston: Academic Press 2014; pp. 581-94.
[http://dx.doi.org/10.1016/B978-0-12-398358-9.00030-6]
[48]
Abujarour R, Bennett M, Valamehr B, et al. Myogenic differentiation of muscular dystrophy-specific induced pluripotent stem cells for use in drug discovery. Stem Cells Transl Med 2014; 3(2): 149-60.
[http://dx.doi.org/10.5966/sctm.2013-0095] [PMID: 24396035]
[49]
Lian Q, Zhang Y, Zhang J, et al. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 2010; 121(9): 1113-23.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.898312]
[50]
Naldini L. Gene therapy returns to centre stage. Nature 2015; 526(7573): 351-60.
[http://dx.doi.org/10.1038/nature15818] [PMID: 26469046]
[51]
Ginn SL, Amaya AK, Alexander IE, Edelstein M, Abedi MR. Gene therapy clinical trials worldwide to 2017: An update. J Gene Med 2018; 20(5): e3015
[http://dx.doi.org/10.1002/jgm.3015] [PMID: 29575374]
[52]
Guan X, Goddard MA, Mack DL, Childers MK. Gene therapy in monogenic congenital myopathies.In: Childers MK, Ed. . Translating regenerative medicine to the clinic. Boston: Academic Press 2016; pp. 203-14.
[http://dx.doi.org/10.1016/B978-0-12-800548-4.00013-9]
[53]
Bartoli M, Gicquel E, Barrault L, et al. Mannosidase I inhibition rescues the human α-sarcoglycan R77C recurrent mutation. Hum Mol Genet 2008; 17(9): 1214-21.
[http://dx.doi.org/10.1093/hmg/ddn029] [PMID: 18252745]
[54]
Gastaldello S, D’Angelo S, Franzoso S, et al. Inhibition of proteasome activity promotes the correct localization of disease-causing α-sarcoglycan mutants in HEK-293 cells constitutively expressing β-, γ-, and δ-sarcoglycan. Am J Pathol 2008; 173(1): 170-81.
[http://dx.doi.org/10.2353/ajpath.2008.071146] [PMID: 18535179]
[55]
Malcher J, Heidt L, Goyenvalle A, et al. Exon skipping in a dysf-missense mutant mouse model. Mol Ther Nucleic Acids 2018; 13: 198-207.
[http://dx.doi.org/10.1016/j.omtn.2018.08.013] [PMID: 30292141]
[56]
Thomas PJ, Xu R, Martin PT. B4GALNT2 (GALGT2) gene therapy reduces skeletal muscle pathology in the FKRP P448L mouse model of limb girdle muscular dystrophy 2I. Am J Pathol 2016; 186(9): 2429-48.
[http://dx.doi.org/10.1016/j.ajpath.2016.05.021] [PMID: 27561302]
[57]
El-Battrawy I, Zhao Z, Lan H, et al. Ion channel dysfunctions in dilated cardiomyopathy in limb-girdle muscular dystrophy. Circ Genom Precis Med 2018; 11(3): e001893
[http://dx.doi.org/10.1161/CIRCGEN.117.001893] [PMID: 29545480]
[58]
Turan S, Farruggio AP, Srifa W, Day JW, Calos MP. Precise correction of disease mutations in induced pluripotent stem cells derived from patients with limb girdle muscular dystrophy. Mol Ther 2016; 24(4): 685-96.
[http://dx.doi.org/10.1038/mt.2016.40]
[59]
Wallace LM, Giesige CR, Griffin DA, Rodino-Klapaca LR, Harper SQ. RNAi therapy for dominant limb girdle muscular dystrophy type 1A. Mol Ther 2016; 24: S248.
[http://dx.doi.org/10.1016/S1525-0016(16)33433-5]
[60]
Bartoli M, Roudaut C, Martin S, et al. Safety and efficacy of AAV-mediated calpain 3 gene transfer in a mouse model of limb-girdle muscular dystrophy type 2A. Mol Ther 2006; 13(2): 250-9.
[http://dx.doi.org/10.1016/j.ymthe.2005.09.017] [PMID: 16290124]
[61]
Prahm KP, Feldt-Rasmussen U, Vissing J. Human growth hormone stabilizes walking and improves strength in a patient with dominantly inherited calpainopathy. Neuromuscul Disord 2017; 27(4): 358-62.
[http://dx.doi.org/10.1016/j.nmd.2017.01.015] [PMID: 28190647]
[62]
Ohsawa Y, Nishimatsu S, Fujino M, Sunada Y. Targeting the type I TGF-β receptor for treating Caveolin-3-Deficient autosomal dominant limb-girdle muscular dystrophy type 1C and muscle wasting disorders.In: Takeda S, Miyagoe-Suzuki Y, Mori-Yoshimura M. Eds., . Translational research in muscular dystrophy. Tokyo: Springer 2016; pp. 77-86.
[63]
Herson S, Hentati F, Rigolet A, et al. A phase I trial of adeno-associated virus serotype 1-γ-sarcoglycan gene therapy for limb girdle muscular dystrophy type 2C. Brain 2012; 135(Pt 2): 483-92.
[http://dx.doi.org/10.1093/brain/awr342] [PMID: 22240777]
[64]
Gao QQ, Wyatt E, Goldstein JA, et al. Reengineering a transmembrane protein to treat muscular dystrophy using exon skipping. J Clin Invest 2015; 125(11): 4186-95.
[http://dx.doi.org/10.1172/JCI82768] [PMID: 26457733]
[65]
Pozsgai ER, Griffin DA, Heller KN, Mendell JR, Rodino-Klapac LR. Systemic AAV-Mediated β-Sarcoglycan delivery targeting cardiac and skeletal muscle ameliorates histological and functional deficits in LGMD2E mice. Mol Ther 2017; 25(4): 855-69.
[http://dx.doi.org/10.1016/j.ymthe.2017.02.013] [PMID: 28284983]
[66]
Nicolson SC, Li C, Hirsch ML, Setola V, Samulski RJ. Identification and validation of small molecules that enhance recombinant adeno-associated virus transduction following high-throughput screens. J Virol 2016; 90(16): 7019-31.
[http://dx.doi.org/10.1128/JVI.02953-15] [PMID: 27147738]
[67]
Yang GS, Schmidt M, Yan Z, et al. Virus-mediated transduction of murine retina with adeno-associated virus: effects of viral capsid and genome size. J Virol 2002; 76(15): 7651-60.
[http://dx.doi.org/10.1128/JVI.76.15.7651-7660.2002] [PMID: 12097579]
[68]
Mendell JR, Chicoine LG, Al-Zaidy SA, et al. Gene delivery for limb-girdle muscular dystrophy type 2D by isolated limb infusion. Hum Gene Ther 2019; 30(7): 794-801.
[http://dx.doi.org/10.1089/hum.2019.006] [PMID: 30838895]
[69]
Brockington M, Blake DJ, Prandini P, et al. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin α2 deficiency and abnormal glycosylation of α-dystroglycan. Am J Hum Genet 2001; 69(6): 1198-209.
[http://dx.doi.org/10.1086/324412] [PMID: 11592034]
[70]
Gicquel E, Maizonnier N, Foltz SJ, et al. AAV-mediated transfer of FKRP shows therapeutic efficacy in a murine model but requires control of gene expression. Hum Mol Genet 2017; 26(10): 1952-65.
[http://dx.doi.org/10.1093/hmg/ddx066] [PMID: 28334834]
[71]
Kunkel SD, Suneja M, Ebert SM, et al. mRNA expression signatures of human skeletal muscle atrophy identify a natural compound that increases muscle mass. Cell Metab 2011; 13(6): 627-38.
[http://dx.doi.org/10.1016/j.cmet.2011.03.020] [PMID: 21641545]
[72]
Swierczek M, Izsvák Z, Ivics Z. The Sleeping Beauty transposon system for clinical applications. Expert Opin Biol Ther 2012; 12(2): 139-53.
[http://dx.doi.org/10.1517/14712598.2012.642358] [PMID: 22176302]
[73]
Escobar H, Schöwel V, Spuler S, Marg A, Izsvák Z. Full-length dysferlin transfer by the hyperactive sleeping beauty transposase restores dysferlin-deficient muscle. Mol Ther Nucleic Acids 2016; 5: e277
[http://dx.doi.org/10.1038/mtna.2015.52] [PMID: 26784637]
[74]
Moldt B, Miskey C, Staunstrup NH, et al. Comparative genomic integration profiling of Sleeping Beauty transposons mobilized with high efficacy from integrase-defective lentiviral vectors in primary human cells. Mol Ther 2011; 19(8): 1499-510.
[http://dx.doi.org/10.1038/mt.2011.47] [PMID: 21468003]
[75]
Weisleder N, Takeshima H, Ma J. Mitsugumin 53 (MG53) facilitates vesicle trafficking in striated muscle to contribute to cell membrane repair. Commun Integr Biol 2009; 2(3): 225-6.
[http://dx.doi.org/10.4161/cib.2.3.8077] [PMID: 19641737]
[76]
Gushchina LV, Bhattacharya S, McElhanon KE, et al. Treatment with recombinant human MG53 protein increases membrane integrity in a mouse model of limb girdle muscular dystrophy 2B. Mol Ther 2017; 25(10): 2360-71.
[http://dx.doi.org/10.1016/j.ymthe.2017.06.025] [PMID: 28750735]
[77]
Aartsma-Rus A, Singh KH, Fokkema IF, et al. Therapeutic exon skipping for dysferlinopathies? Eur J Hum Genet 2010; 18(8): 889-94.
[http://dx.doi.org/10.1038/ejhg.2010.4] [PMID: 20145676]
[78]
Aartsma-Rus A. Overview on DMD exon skipping. Methods Mol Biol 2012; 867: 97-116.
[http://dx.doi.org/10.1007/978-1-61779-767-5_7]
[79]
Sinnreich M, Therrien C, Karpati G. Lariat branch point mutation in the dysferlin gene with mild limb-girdle muscular dystrophy. Neurology 2006; 66(7): 1114-6.
[http://dx.doi.org/10.1212/01.wnl.0000204358.89303.81] [PMID: 16606933]
[80]
Evers MM, Toonen LJA, van Roon-Mom WMC. Antisense oligonucleotides in therapy for neurodegenerative disorders. Adv Drug Deliv Rev 2015; 87: 90-103.
[http://dx.doi.org/10.1016/j.addr.2015.03.008] [PMID: 25797014]
[81]
Barthélémy F, Blouin C, Wein N, et al. Exon 32 skipping of dysferlin rescues membrane repair in patients’ cells. J Neuromuscul Dis 2015; 2(3): 281-90.
[http://dx.doi.org/10.3233/JND-150109] [PMID: 27858744]
[82]
Wilton SD, Fall AM, Harding PL, McClorey G, Coleman C, Fletcher S. Antisense oligonucleotide-induced exon skipping across the human dystrophin gene transcript. Mol Ther 2007; 15(7): 1288-96.
[http://dx.doi.org/10.1038/sj.mt.6300095] [PMID: 17285139]
[83]
Aartsma-Rus A, Krieg AM. FDA approves eteplirsen for duchenne muscular dystrophy: The next chapter in the eteplirsen saga. Nucleic Acid Ther 2017; 27(1): 1-3.
[http://dx.doi.org/10.1089/nat.2016.0657] [PMID: 27929755]
[84]
Kole R, Krainer AR, Altman S. RNA therapeutics: beyond RNA interference and antisense oligonucleotides. Nat Rev Drug Discov 2012; 11: 125.
[http://dx.doi.org/10.1038/nrd3625]
[85]
Davidson BL, McCray PB Jr. Current prospects for RNA interference-based therapies. Nat Rev Genet 2011; 12(5): 329-40.
[http://dx.doi.org/10.1038/nrg2968] [PMID: 21499294]
[86]
Khan T, Weber H, DiMuzio J, et al. Silencing myostatin using cholesterol-conjugated siRNAs induces muscle growth. Mol Ther Nucleic Acids 2016; 5(8): e342
[http://dx.doi.org/10.1038/mtna.2016.55] [PMID: 27483025]
[87]
Khadempar S, Familghadakchi S, Motlagh RA, et al. CRISPR-Cas9 in genome editing: Its function and medical applications. J Cell Physiol 2019; 234(5): 5751-61.
[http://dx.doi.org/10.1002/jcp.27476] [PMID: 30362544]
[88]
Long C, Amoasii L, Bassel-Duby R, Olson EN. Genome editing of monogenic neuromuscular diseases: A systematic review. JAMA Neurol 2016; 73(11): 1349-55.
[http://dx.doi.org/10.1001/jamaneurol.2016.3388] [PMID: 27668807]
[89]
Turan S, Farruggio AP, Srifa W, Day JW, Calos MP. Precise correction of disease mutations in induced pluripotent stem cells derived from patients with limb girdle muscular dystrophy. Mol Ther 2016; 24(4): 685-96.
[http://dx.doi.org/10.1038/mt.2016.40] [PMID: 26916285]

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